Chemodiverse cell systems responses to UV in an algal sister of land plants

Abstract

Plant terrestrialization necessitated that a barrage of stressors had to be overcome1. Land plants use an integrated response network in adjusting their molecular physiology to terrestrial stressors2--one of the foremost being UV irradiance. The zygnematophytes are the closest streptophyte algal relatives of land plants3-5, are renowned for their resilience to UV stress6-8, and thus allow to glean key information for inferring the UV response toolkit of the earliest land plants9,10. Throughout streptophyte evolution, specialised metabolism radiated into creating diverse compounds used for responses to environmental challenges, such as sun-shielding compounds and antioxidants11-14. This includes UV-shielding compounds like flavonoids and coumarins but also the land plant specific polymer lignin, giving structural support in vascular plants15; homologs of the underpinning core pathway occur in streptophyte algae16. Here, we exposed the zygnematophyte Mesotaenium to UV-B irradiation and profiled its physiology, morphology, transcriptomics as well as metabolomic features. After UV-B exposure, cells showed rapid photophysiological responses and progressively growing terminal vacuoles. Our transcriptome data capture dynamic changes in gene expression of (i) core downstream responses such as genes homologous to phenol metabolic enzymes, photophysiological homeostats, and DNA repair factors; but also (ii) upstream components featuring key homologs of kinase-mediated signalling cascades, as well as light quality and abscisic acid-mediated signalling components. To scrutinize the acclimatory chassis, we created a metabolite feature database specifically for the Mesotaenium metabolome. Upon UV-B exposure, the metabolome displayed pronounced temporal shifts, with several phenolic features that accumulate along the stress-acclimation kinetics. Overall, we capture a chemodiverse response including various phenolics such as purpurogallin-like, methoxypsoralen-like derivatives and coumarins. Our data establish an integrated model for UV responses in the closest algal relatives of land plants, shedding light on the toolkit that allowed the progenitors of land plants to move out of a protective water column.